Incidence,Risk Factors,and Outcomes of Central Line-Associated Bloodstream Infections in Trauma Patients

Abstract

Introduction:

Central line-associated blood stream infection (CLABSI) is a hospital-acquired infection (HAI) associated with increased morbidity and mortality among the general patient population. However, few studies have evaluated the incidence, outcomes, and risk factors for CLABSI in trauma patients. This study aimed to identify the rate of positive (+)CLABSI in trauma patients and risk factors associated with (+)CLABSI.

Methods:

The 2017–2021 Trauma Quality Improvement Program database was queried for trauma patients aged ≥18 years undergoing central-line placement. We compared patients with (+)CLABSI vs. (−)CLABSI patients. Bivariate and multivariable logistic regression analyses were performed.

Results:

From 175,538 patients undergoing central-line placement, 469 (<0.1%) developed CLABSI. The (+)CLABSI patients had higher rates of cirrhosis (3.9% vs. 2.0%, p = 0.003) and chronic kidney disease (CKD) (4.3% vs. 2.6%, p = 0.02). The (+)CLABSI group had increased injury severity score (median: 25 vs. 13, p < 0.001), length of stay (LOS) (median 33.5 vs. 8 days, p < 0.001), intensive care unit LOS (median 21 vs. 6 days, p < 0.001), and mortality (23.7% vs. 19.6%, p = 0.03). Independent associated risk factors for (+)CLABSI included catheter-associated urinary tract infection (CAUTI) (odds ratio [OR] = 5.52, confidence interval [CI] = 3.81–8.01), ventilator-associated pneumonia (VAP) (OR = 4.43, CI = 3.42–5.75), surgical site infection (SSI) (OR = 3.66, CI = 2.55–5.25), small intestine injury (OR = 1.91, CI = 1.29–2.84), CKD (OR = 2.08, CI = 1.25–3.47), and cirrhosis (OR = 1.81, CI = 1.08–3.02) (all p < 0.05).

Conclusion:

Although CLABSI occurs in <0.1% of trauma patients with central-lines, it significantly impacts LOS and morbidity/mortality. The strongest associated risk factors for (+)CLABSI included HAIs (CAUTI/VAP/SSI), specific injuries (small intestine), and comorbidities. Providers should be aware of these risk factors with efforts made to prevent CLABSI in these patients.

Introduction

Hospital-acquired infections (HAIs), notably surgical site infections (SSIs), catheter-associated urinary tract infections (CAUTI), ventilator-associated pneumonia (VAP), and central line-associated bloodstream infections (CLABSI), represent a pivotal challenge in healthcare, affecting patient safety and clinical outcomes. The prevention of these HAIs is a paramount concern for healthcare providers, particularly surgeons, given the inherent risks associated with surgical interventions.^1–5 Despite evidence suggesting that up to one-third of HAIs are preventable, they persist as a leading contributor to increased hospital length of stay (LOS), morbidity, and mortality in hospitalized patients.⁶

Central venous catheters (CVCs) are important devices for trauma patients, used to facilitate the delivery of medications (e.g., vasopressors, hypertonic saline etc.), rapidly transfuse blood products in the setting of massive hemorrhage, and facilitate hemodialysis when acute renal failure occurs.⁷ However, CVCs expose patients to the risk of CLABSI, defined as bloodstream infections associated with a current or recently used CVC in the absence of infections at any other site.⁸ The risk factors for developing CLABSI are multifaceted, encompassing the CVC’s location, duration of use (catheter days), patient demographics (including age, severity of illness, and immune status), catheter type (tunneled vs. non-tunneled or venous vs. arterial), and the effectiveness of a hospital’s infection control practices.^9–12 Despite numerous efforts to reduce their incidence, CLABSIs continue to pose a significant threat to patient safety.¹³

The body of research on CLABSI has predominantly focused on general hospital populations, with a paucity of data specifically addressing the unique characteristics and needs of trauma patients. This population presents distinct demographics, HAI profiles, types of injuries, and modifiable risk factors that may be associated with CLABSI.¹⁴ As such, this study aimed to elucidate the incidence of CLABSI within a national trauma cohort and identify risk factors associated with CLABSI. This may help inform prognostication of patient outcomes and/or be utilized for quality improvement strategies to curtail the risk of CLABSI in trauma care, thereby enhancing the overall quality and safety of patient treatment.

Methods

This study was approved by our Institutional Review Board, and a waiver of consent was granted as it utilizes a national de-identified database. The 2017–2021 Trauma Quality Improvement Program (TQIP) database was queried for trauma patients 18 years of age and older who underwent central-line placement during hospitalization. Patients transferred from another hospital were excluded.

Patients were categorized into two groups: those who developed a CLABSI [(+)CLABSI] following central-line placement and those who did not [(−)CLABSI]. The definition of CLABSI used in this study aligns with the criteria set forth by the Centers for Disease Control and Prevention, detailed in Supplementary Appendix S1. Outcomes measured included hospital LOS, intensive care unit (ICU) LOS, ventilator days, and in-hospital complications including SSI, VAP, and CAUTI. Demographic variables collected for this study included age, gender, vitals on arrival, and comorbidities including cerebrovascular accident (CVA), chronic obstructive pulmonary disease (COPD), chronic kidney disease (CKD), cirrhosis, diabetes, and data on smoking, alcohol, substance, and steroid use. The injury profile collected included the mechanism of injury, injury severity score (ISS), and incidences of injuries to specific organs including the brain, ribs, lungs, stomach, small intestine, colon, and rectum.

Bivariate analyses were performed utilizing the Mann–Whitney U test and Pearson’s chi-squared analysis to compare continuous and categorical variables, respectively. Continuous variables were reported as medians with an interquartile range, and categorical variables as frequencies. Following a collaborative discussion among coauthors and a review of the literature, we selected variables available within TQIP that may be linked to CLABSI.^15,16 These variables were initially analyzed using a univariable logistic regression model. Those with a p-value less than 0.20 were subsequently included in a multivariable logistic regression analysis. The adjusted risk for (+)CLABSI was evaluated using a hierarchical multivariable logistic regression model, which reported the results as odds ratio (OR) with a 95% confidence interval (CI). To assess the discriminative ability of our logistic regression model, we calculated the C-statistic, derived from the area under the receiver operating characteristic curve. The C-statistic value obtained was 0.796, indicating good discriminative ability of the model to correctly classify cases with and without CLABSI. Furthermore, to evaluate the goodness-of-fit of the model, the Hosmer–Lemeshow test was used, resulting in a chi-square value of 23.119 with 8 degrees of freedom and a significance level of 0.184. This indicates a satisfactory alignment between the observed outcomes and the predictions made by the model. All analyses were two-sided and were conducted using IBM SPSS Statistics for Windows (version 28; IBM Corporation, Armonk, NY), with a statistical significance set at p < 0.05.

Results

Demographics, vitals, and comorbidities of (+)CLABSI vs. (−)CLABSI

From 175,538 trauma patients undergoing central-line placement, 469 (<0.1%) developed CLABSI during hospitalization. Compared to patients with (−)CLABSI, patients with (+)CLABSI were younger (median age, 48 vs. 52, p = 0.02) and had a higher proportion of males (76.3% vs. 67.2%, p < 0.001). The majority of comorbidities were similar between cohorts, except the (+)CLABSI group had higher rates of cirrhosis (3.9% vs. 2.0%, p = 0.003), CKD (4.3% vs. 2.6%, p = 0.02), and alcohol use (12.2% vs. 7.7%, p < 0.001) (Table 1).

Table 1.

Demographics, Comorbidities, and Vital Signs for Trauma Patients with a Central-Line with Positive CLABSI and No CLABSI

	CLABSI (−)	CLABSI (+)
Characteristic	(n = 175,069)	(n = 469)	p
Age, year, median (IQR)	52 (32, 68)	48 (32, 64)	0.02
Male, n (%)	117,362 (67.2%)	358 (76.3%)	<0.001
Comorbidities, n (%)
Cerebrovascular accident	4,535 (2.6%)	11 (2.4%)	0.73
COPD	12,216 (7.1%)	36 (7.8%)	0.57
Cirrhosis	3,403 (2.0%)	18 (3.9%)	0.003
Chronic kidney disease	4,476 (2.6%)	20 (4.3%)	0.02
Diabetes	24,960 (14.5%)	70 (15.2%)	0.71
Disseminated cancer	1,116 (0.7%)	3 (0.7%)	0.10
Currently on chemotherapy	817 (0.5%)	1 (0.2%)	0.42
Steroid use	1,426 (0.8%)	8 (1.7%)	0.03
Substance use	14,566 (8.5%)	46 (10.0%)	0.25
Alcohol use disorder	13,208 (7.7%)	56 (12.2%)	<0.001
Smoker	35,767 (20.8%)	86 (18.7%)	0.25
Vitals on admission, n (%)
Hypotensive (SBP < 90 mmHg)	22,292 (13.0%)	82 (18.1%)	0.002
Tachycardia (HR > 120/min)	25,815 (15.0%)	136 (29.5%)	<0.001
Tachypnea (RR > 22/min)	41,996 (25.1%)	138 (31.9%)	0.001

CLABSI = central line-associated bloodstream infection; IQR = interquartile range; COPD = chronic obstructive pulmonary disease; SBP = systolic blood pressure; HR = heart rate; RR = respiratory rate.

Injury profile of (+)CLABSI vs. (−)CLABSI

The (+)CLABSI cohort had a higher median ISS (25 vs. 13, p < 0.001) compared to the (−)CLABSI group. Except for a similar rate of injury to the stomach, the (+)CLABSI cohort had increased rates of brain injury (40.3% vs. 30.0%), rib fractures (47.3% vs. 27.8%), as well as injuries to the lung (45.8% vs. 26.9%), liver (15.6% vs. 7.8%), small intestine (10.0% vs. 3.8%), colon (9.6% vs. 3.5%), and rectum (1.5% vs. 0.4%) (all p < 0.001) (Table 2).

Table 2.

Injury Profile for Trauma Patients with a Central-Line with Positive CLABSI and No CLABSI

	CLABSI (−)	CLABSI (+)
Characteristic	(n = 175,069)	(n = 469)	p
ISS, median (IQR)	13 (5, 25)	25 (16, 34)	<0.001
Injuries, n (%)
Brain	52,529 (30.0%)	189 (40.3%)	<0.001
Rib fracture	48,633 (27.8%)	222 (47.3%)	<0.001
Lung	47,172 (26.9%)	215 (45.8%)	<0.001
Stomach	1,936 (1.1%)	9 (1.9%)	0.09
Liver	13,601 (7.8%)	73 (15.6%)	<0.001
Small intestine	6,615 (3.8%)	47 (10.0%)	<0.001
Colon	6,142 (3.5%)	45 (9.6%)	<0.001
Rectum	652 (0.4%)	7 (1.5%)	<0.001
Penetrating mechanism	27,587 (15.8%)	49 (10.4%)	0.002

CLABSI = central line associated blood stream infection; ISS = injury severity score; IQR = interquartile range.

Clinical outcomes for (+)CLABSI vs. (−)CLABSI

Patients in the (+)CLABSI group had increased mortality compared with the (−)CLABSI cohort (23.7% vs. 19.6%, p = 0.03). The (+)CLABSI cohort also had increased LOS (median days: 33.5 vs. 8), ICU LOS (median days: 21 vs. 6), ventilator days (median 16 vs. 5), and all in-hospital complications including SSI (8.5% vs. 1.3%), VAP (22.8% vs. 2.9%), and CAUTI (9.6% vs. 0.8%) (all p < 0.001) (Table 3).

Table 3.

Clinical Outcomes and Complications for Trauma Patients with a Central Line with Positive CLABSI and No CLABSI

	CLABSI (−)	CLABSI (+)
Characteristic	(n = 175,069)	(n = 469)	p
Hospital LOS, days, median (IQR)	8 (3, 17)	33.5 (23, 53)	<0.001
ICU LOS, days, median (IQR)	6 (3, 13)	21 (14, 33)	<0.001
Ventilator, days, median (IQR)	5 (2, 11)	16 (9, 28)	<0.001
Complications, n (%)
Surgicalsite infection	2,205 (1.3%)	40 (8.5%)	<0.001
Ventilator-associated pneumonia	5,125 (2.9%)	105 (22.8%)	<0.001
CAUTI	1,365 (0.8%)	44 (9.6%)	<0.001
Mortality	34,331 (19.6%)	111 (23.7%)	0.03

CLABSI = central line associated blood stream infection; ICU = intensive care unit; LOS = length of stay; IQR = interquartile range; CAUTI = catheter-associated urinary tract infection.

Multivariable logistic regression analysis for risk of CLABSI

On multivariable analysis, independent associated risk factors for (+)CLABSI included ISS (OR = 1.03, CI = 1.02–1.03), CAUTI (OR = 5.52, CI = 3.81–8.01), VAP (OR = 4.43, CI = 3.42–5.75), SSI (OR = 3.66, CI = 2.55–5.25), small intestine injury (OR = 1.91, CI = 1.29–2.84), CKD (OR = 2.08, CI = 1.25–3.47), cirrhosis (OR = 1.81, CI = 1.08–3.02), and alcohol use disorder (OR = 1.45, CI = 1.05–2.01) (all p < 0.05) (Table 4).

Table 4.

Multivariable Logistic Regression for Associated Risk of CLABSI

Predictors of CLABSI^a	OR	CI	p
Injury severity score	1.03	1.02–1.03	<0.001
Comorbidities
Cerebrovascular accident	0.99	0.50–1.94	0.97
Chronic obstructive pulmonary disease	1.39	0.96–2.02	0.08
Cirrhosis	1.81	1.08–3.02	0.02
Chronic kidney disease	2.08	1.25–3.47	0.005
Diabetes	1.07	0.80–1.45	0.64
Currently on chemotherapy	0.66	0.09–4.86	0.68
Steroid use	1.85	0.81–4.23	0.14
Alcohol use disorder	1.45	1.05–2.01	0.03
Smoker	0.79	0.61–1.03	0.09
Injuries
Brain	1.92	0.73–1.14	0.44
Stomach	1.07	0.51–2.28	0.86
Liver	1.14	0.84–1.53	0.40
Small intestine	1.91	1.29–2.84	<0.001
Colon	1.43	0.96–2.15	0.08
Rectum	2.15	0.93–4.97	0.08
Surgical-site infection	3.66	2.55–5.25	<0.001
Ventilator-associated pneumonia	4.43	3.42–5.75	<0.001
CAUTI	5.52	3.81–8.01	<0.001

CLABSI = central line-associated bloodstream infection; CAUTI = catheter-associated urinary tract infection.

Controlling for age ≥ 65, male gender, hypotension on arrival (systolic blood pressure <90 mmHg), tachycardia on arrival (heart rate >90 beats per minute), tachypnea on arrival (respiratory rate >22 breaths per minute), disseminated cancer, substance use, rib fracture, lung injury, and penetrating mechanism of injury.

Discussion

Use of CVCs are important for the resuscitation and care of trauma patients.¹⁷ This national analysis spanning four years of data found the incidence of CLABSI is quite low for trauma patients. However, the (+)CLABSI patients experienced higher mortality rates, along with increased hospital and ICU LOS. In addition, some HAIs such as SSI, VAP, and CAUTI, were identified as significant associated risk factors, elevating the likelihood of developing CLABSI by nearly fourfold or higher. Interestingly, our analysis also demonstrated comorbidities (i.e., cirrhosis and CKD) as well as injuries to the small intestine to be associated with (+)CLABSI.

The development of CLABSI can have significant consequences not only for the patient but also for the institution or hospital. Previous studies have demonstrated an association between CLABSI and both increased mortality and hospital LOS in generalized populations.^7,11,18 Chovanec et al. found that among hospitalized patients, those with CLABSI had a 36% increased likelihood of mortality during hospitalization, along with an additional average of two days of hospital LOS.¹⁸ In a single-center study of ICU-admitted patients, Burden et al. found an increase in both hospital and ICU LOS for (+)CLABSI patients, with ICU stays ranging between 16 and 29 days for those with CLABSI, compared with just 4–5 days for those without.¹⁹ This is a significant impact on the hospital and patient, as each ICU day can cost between $3970 and $6853.²⁰ Our national analysis demonstrated that trauma patients with CLABSI also experienced significantly higher mortality and longer hospital and ICU stays, aligning with these prior smaller studies. This highlights the importance of future CLABSI prevention efforts in the trauma population.

The presence of HAIs, such as SSI, VAP, and CAUTI, and their impact on developing CLABSI remains a significant concern among healthcare providers. A common cause of developing HAIs like CLABSI, VAP, and CAUTI is the prolonged use of invasive devices among hospitalized patients.^21,22 These devices can create an environment ideal for biofilm formation, which can disrupt antibiotic penetration, leading to higher antibiotic usage and resistance, therefore increasing the risk of CLABSI.^21,22 Although reducing catheter days can lower CLABSI incidence, the essential use of catheters in clinical care necessitates the adoption of diverse strategies for reduction of CLABSIs. Additionally, the extensive use of antibiotic treatments can also lead to antibiotic resistance, further complicating the management of CLABSI.²³ Our study demonstrated that HAIs such as CAUTI, VAP, and SSI were associated with increased risk of CLABSI development by nearly fourfold or higher. This highlights the importance of preventive strategies such as prompt removal of urinary catheters, early liberation from mechanical ventilation, and the implementation of care bundles to lower the risk of all HAIs.^1,24,25 Enhancing immune function may also be beneficial as an additional preventive measure, given the increased risk of CLABSI in immunocompromised populations; however, this approach merits further research.¹¹

Optimal prevention of CLABSI requires targeted interventions for those at highest risk. The greatest risk factor for CLABSI is the presence of a CVC. In addition, there may be an increased risk of CLABSI with the use of multiple catheters,¹¹ however, this might reflect selection bias, and thus requires future prospective randomized controlled trials to confirm this finding. This study adds to known efforts by identifying injury patterns at higher risk for CLABSI, who should avoid CVCs whenever possible. Our data expand upon work by Hessels et al., who demonstrated that trauma patients with abdominal and pelvic injuries are more susceptible to HAIs.²⁶ In addition, both Komori et al. and Kaufman et al. identified higher rates of HAIs in patients with abdominal injuries.^27,28 Our study provides more granular data than these prior studies by identifying injuries to the small intestine as an independent associated risk factor for CLABSI. This may be expected as the concentration of microorganisms increase in the intestinal portions of the gastrointestinal tract (from 10⁴ organisms/g in the stomach to 10⁸ organisms/g in the small intestine).²⁹ This highlights the need for careful consideration for the placement of central-lines in this population and/or early removal. The integration of these findings into trauma care protocols could lead to improved patient outcomes by decreasing the risk of CLABSI in trauma patients, and thereby reducing morbidity and mortality.

Limitations of this study include those inherent to its retrospective database design, such as missing data, coding errors, as well as selection and reporting bias. Another notable limitation is the lack of detailed information regarding the specific duration (catheter days) and management of central-line placements in trauma patients. Additionally, this study is unable to discern the timing or sequence of complications such as CAUTI and VAP in relation to CLABSI, which complicates determining whether these are causative or reactive, and whether interventions for one infection might precipitate another, highlighting the need for future prospective multicenter studies to clarify these dynamics. Moreover, this study is unable to determine whether extended LOS and mechanical ventilation are risk factors for CLABSI or consequences of it. In short, the retrospective database design of our analysis limits our ability to establish causality between these or any identified risk factors. Also, the cause of death for patients is not detailed within TQIP, which could provide further insight into the direct and indirect impacts of CLABSI. In addition, the TQIP database does not include specific data on the duration of catheter use, limiting our study’s ability to reach comprehensive conclusions regarding CLABSI incidence as related to the more informative variable of catheter days, again highlighting the necessity for future prospective multicenter studies. Finally, the TQIP database only includes index hospitalization data and thus may underestimate the long-term morbidity and mortality associated with CLABSI.

Conclusion

This national analysis spanning four years of data found that the incidence of CLABSI in trauma patients with CVCs was rare (<0.1%). The presence of other HAIs like CAUTI, VAP, and SSI were found to be associated risk factors for CLABSI by nearly four times or greater. Importantly, our study also identified specific organ injuries (small intestine), as key risk factors for CLABSI in trauma patients. These findings highlight the critical importance of refining infection control protocols in trauma settings, especially for those with significant risk factors identified in this study. Future prospective quality improvement research is needed to determine whether targeted prevention efforts for high-risk patients identified in this study can further decrease the incidence of CLABSI and thereby improve outcomes.

Footnotes

Author Disclosure Statement

The authors declare that there is no conflict of interest.

Funding Information

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Supplementary Material

References

Dellinger

. Prevention of hospital-acquired infections. Surg Infect (Larchmt), 2016; 17(4):422–426; doi: 10.1089/sur.2016.048

Lem

, Jasperse

, Grigorian

, et al. Effect of external urinary collection device implementation on female surgical patients. Infect Dis Health, 2022; 27(4):227–234; doi: 10.1016/j.idh.2022.05.005

Geffers

, Sohr

, Gastmeier

. Mortality attributable to hospital-acquired infections among surgical patients. Infect Control Hosp Epidemiol, 2008; 29(12):1167–1170; doi: 10.1086/592410

Korol

, Johnston

, Waser

, et al. A systematic review of risk factors associated with surgical site infections among surgical patients. PLoS One, 2013; 8(12):e83743; doi: 10.1371/journal.pone.0083743

Krein

, Kowalski

, Hofer

, et al. Preventing hospital-acquired infections: A national survey of practices reported by U.S. Hospitals in 2005 and 2009. J Gen Intern Med, 2012; 27(7):773–779; doi: 10.1007/s11606-011-1935-y

Tariq

, Lancaster

, Elugunti

, et al. Graph convolutional network-based fusion model to predict risk of hospital acquired infections. J Am Med Inform Assoc, 2023; 30(6):1056–1067; doi: 10.1093/jamia/ocad045

Foka

, Nicolaou

, Kyprianou

, et al. Prevention of central line-associated bloodstream infections through educational interventions in adult intensive care units: A systematic review. Cureus, 2021; 13(8):e17293; doi: 10.7759/cureus.17293

Larsen

, Gavin

, Marsh

, et al. A systematic review of central-line–associated bloodstream infection (CLABSI) diagnostic reliability and error. Infect Control Hosp Epidemiol, 2019; 40(10):1100–1106; doi: 10.1017/ice.2019.205

Lobdell

, Stamou

, Sanchez

. Hospital-Acquired Infections. Surg Clin North Am, 2012; 92(1):65–77; doi: 10.1016/j.suc.2011.11.003

10.

Moriyama

, Ando

, Kotani

, et al. Risk factors associated with increased incidences of catheter-related bloodstream infection. Medicine (Baltimore), 2022; 101(42):e31160; doi: 10.1097%2FMD.0000000000031160

11.

Alshahrani

, Alhuwaishel

, Alangari

, et al. Clinical impacts and risk factors for central line-associated bloodstream infection: A systematic review. Cureus, 2023; 15(6):e40954; doi: 10.7759/cureus.40954

12.

Maqbool

, Sharma

. A two-year surveillance of central line-associated bloodstream infections in the trauma ICU of a tertiary care hospital in India. Cureus, 2023; 15(9):e45325; doi: 10.7759%2Fcureus.45325

13.

Rahmani

, Garikipati

, Barnes

, et al. Early prediction of central line associated bloodstream infection using machine learning. Amer J Infection Control, 2022; 50(4):440–445; doi: 10.1016/j.ajic.2021.08.017

14.

Lee

, Krecko

, Savage

, et al. Which hospital-acquired conditions matter the most in trauma? An evidence-based approach for prioritizing trauma program improvement. J Trauma Acute Care Surg, 2022; 93(4):446–452; doi: 10.1097/ta.0000000000003645

15.

Haider

, Hashmi

, Zafar

, et al. Developing best practices to study trauma outcomes in large databases: An evidence-based approach to determine the best mortality risk adjustment model. Journal of Trauma and Acute Care Surgery, 2014; 76(4):1061–1069; doi: 10.1097/ta.0000000000000182

16.

Schluter

. The trauma and injury severity score (TRISS) revised. Injury, 2011; 42(1):90–96; doi: 10.1016/j.injury.2010.08.040

17.

Struck

, Ewens

, Schummer

, et al. Central venous catheterization for acute trauma resuscitation: Tip position analysis using routine emergency computed tomography. J Vasc Access, 2018; 19(5):461–466; doi: 10.1177/1129729818758998

18.

Chovanec

, Arsene

, Gomez

, et al. Association of CLABSI with hospital length of stay, readmission rates, and mortality: A retrospective review. Worldviews Evid Based Nurs, 2021; 18(6):332–338; doi: 10.1111/wvn.12548

19.

Burden

, Torjman

, Dy

, et al. Prevention of central venous catheter-related bloodstream infections: Is it time to add simulation training to the prevention bundle? J Clin Anesth, 2012; 24(7):555–560; doi: 10.1016/j.jclinane.2012.04.006

20.

, Kuznik

, Wang

, et al. Incremental costs associated with length of hospitalization due to viral pneumonia: Impact of intensive care and economic implications of reducing the length of stay in the era of COVID-19. Clinicoecon Outcomes Res, 2020; 12:723–731; doi: 10.2147/ceor.s280461

21.

Divatia

, Pulinilkunnathil

, Myatra

. Nosocomial infections and ventilator-associated pneumonia in cancer patients: Oncologic Critical Care. 2019:1419-39; doi: 10.1007/978-3-319-74588-6_125

22.

Al-Tawfiq

, Tambyah

. Healthcare associated infections (HAI) perspectives. J Infect Public Health, 2014; 7(4):339–344; doi: 10.1016/j.jiph.2014.04.003

23.

Sevin

, Daniau

, Alfandari

, et al. Patterns of antibiotic use in hospital-acquired infections. J Hosp Infect, 2021; 114:104–110; doi: 10.1016/j.jhin.2021.05.008

24.

Patel

, Gupta

, Vaughn

, et al. Review of strategies to reduce central line-associated bloodstream infection (CLABSI) and catheter-associated urinary tract infection (CAUTI) in Adult ICUs. J Hosp Med, 2018; 13(2):105–116; doi: 10.12788/jhm.2856

25.

Maselli

, Restrepo

. Strategies in the prevention of ventilator-associated pneumonia. Ther Adv Respir Dis, 2011; 5(2):131–141; doi: 10.1177/1753465810395655

26.

Hessels

, Kuo

, Ahmed

. Epidemiology and impact of healthcare-associated infections in trauma patients: A national data analysis. Surg Infect (Larchmt), 2020; 21(10):871–876; doi: 10.1089/sur.2019.294

27.

Komori

, Iriyama

, Kainoh

, et al. The impact of infection complications after trauma differs according to trauma severity. Sci Rep, 2021; 11(1):13803; doi: 10.1038/s41598-021-93314-5

28.

Kaufman

, Earl-Royal

, Barie

, et al. Failure to rescue after infectious complications in a statewide trauma system. Surg Infect (Larchmt), 2017; 18(2):89–98; doi: 10.1089/sur.2016.112

29.

Brook

. Microbiology and management of abdominal infections. Dig Dis Sci, 2008; 53(10):2585–2591; doi: 10.1007/s10620-007-0194-6

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